Abstract
The initiation and morphogenesis of cutaneous appendages depend on a series of reciprocal signaling events between the epithelium and mesenchyme of the embryonic skin. In the development of feather germs, early dermal signals induce the formation of epidermal placodes that in turn signal the mesoderm to form dermal condensations immediately beneath them. We find a spatially and temporally restricted pattern of transcription for the genes that encode fibroblast growth factor (FGF) 2 and FGF receptor (FGFR) 1 in developing feather germs of the chicken embryo. FGF-2 expression is restricted to the epidermal placodes, whereas FGFR-1 expression is limited to the dermal condensations. Transcription of these genes could not be detected in skins of scaleless (sc/sc) embryos that fail to develop feathers as a result of an ectodermal defect. Treatment of sc/sc skins with FGF-2 results in the formation of feathers at the site of application of the growth factor and the induced feathers express FGFR-1 in their dermal condensations. Thus, we have established FGF-2 as an epidermal signal in early feather germ formation. The observation that FGF-2 can rescue the mutant phenotype of sc/sc embryos suggests that FGF-2 either is, or is downstream from, the signal that the sc/sc mutant ectoderm fails to generate.
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- Chuong C. M. The making of a feather: homeoproteins, retinoids and adhesion molecules. Bioessays. 1993 Aug;15(8):513–521. doi: 10.1002/bies.950150804. [DOI] [PubMed] [Google Scholar]
- Crossley P. H., Minowada G., MacArthur C. A., Martin G. R. Roles for FGF8 in the induction, initiation, and maintenance of chick limb development. Cell. 1996 Jan 12;84(1):127–136. doi: 10.1016/s0092-8674(00)80999-x. [DOI] [PubMed] [Google Scholar]
- Cunha G. R. Role of mesenchymal-epithelial interactions in normal and abnormal development of the mammary gland and prostate. Cancer. 1994 Aug 1;74(3 Suppl):1030–1044. doi: 10.1002/1097-0142(19940801)74:3+<1030::aid-cncr2820741510>3.0.co;2-q. [DOI] [PubMed] [Google Scholar]
- Dono R., Zeller R. Cell-type-specific nuclear translocation of fibroblast growth factor-2 isoforms during chicken kidney and limb morphogenesis. Dev Biol. 1994 Jun;163(2):316–330. doi: 10.1006/dbio.1994.1151. [DOI] [PubMed] [Google Scholar]
- Fallon J. F., López A., Ros M. A., Savage M. P., Olwin B. B., Simandl B. K. FGF-2: apical ectodermal ridge growth signal for chick limb development. Science. 1994 Apr 1;264(5155):104–107. doi: 10.1126/science.7908145. [DOI] [PubMed] [Google Scholar]
- Goetinck P. F., Sekellick M. J. Observations on collagen synthesis, lattice formation, and morphology of scaleless and normal embryonic skin. Dev Biol. 1972 Aug;28(4):636–648. doi: 10.1016/0012-1606(72)90008-5. [DOI] [PubMed] [Google Scholar]
- Jessell T. M., Melton D. A. Diffusible factors in vertebrate embryonic induction. Cell. 1992 Jan 24;68(2):257–270. doi: 10.1016/0092-8674(92)90469-s. [DOI] [PubMed] [Google Scholar]
- Levin M., Johnson R. L., Stern C. D., Kuehn M., Tabin C. A molecular pathway determining left-right asymmetry in chick embryogenesis. Cell. 1995 Sep 8;82(5):803–814. doi: 10.1016/0092-8674(95)90477-8. [DOI] [PubMed] [Google Scholar]
- Mayerson P. L., Fallon J. F. The spatial pattern and temporal sequence in which feather germs arise in the white Leghorn chick embryo. Dev Biol. 1985 Jun;109(2):259–267. doi: 10.1016/0012-1606(85)90453-1. [DOI] [PubMed] [Google Scholar]
- Niswander L., Jeffrey S., Martin G. R., Tickle C. A positive feedback loop coordinates growth and patterning in the vertebrate limb. Nature. 1994 Oct 13;371(6498):609–612. doi: 10.1038/371609a0. [DOI] [PubMed] [Google Scholar]
- Niswander L., Tickle C., Vogel A., Booth I., Martin G. R. FGF-4 replaces the apical ectodermal ridge and directs outgrowth and patterning of the limb. Cell. 1993 Nov 5;75(3):579–587. doi: 10.1016/0092-8674(93)90391-3. [DOI] [PubMed] [Google Scholar]
- Noji S., Koyama E., Myokai F., Nohno T., Ohuchi H., Nishikawa K., Taniguchi S. Differential expression of three chick FGF receptor genes, FGFR1, FGFR2 and FGFR3, in limb and feather development. Prog Clin Biol Res. 1993;383B:645–654. [PubMed] [Google Scholar]
- Noveen A., Jiang T. X., Ting-Berreth S. A., Chuong C. M. Homeobox genes Msx-1 and Msx-2 are associated with induction and growth of skin appendages. J Invest Dermatol. 1995 May;104(5):711–719. doi: 10.1111/1523-1747.ep12606960. [DOI] [PubMed] [Google Scholar]
- Novel G. Feather pattern stability and reorganization in cultured skin. J Embryol Exp Morphol. 1973 Dec;30(3):605–633. [PubMed] [Google Scholar]
- Pasquale E. B., Singer S. J. Identification of a developmentally regulated protein-tyrosine kinase by using anti-phosphotyrosine antibodies to screen a cDNA expression library. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5449–5453. doi: 10.1073/pnas.86.14.5449. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Patterson L. T., Dressler G. R. The regulation of kidney development: new insights from an old model. Curr Opin Genet Dev. 1994 Oct;4(5):696–702. doi: 10.1016/0959-437x(94)90136-q. [DOI] [PubMed] [Google Scholar]
- Perantoni A. O., Dove L. F., Karavanova I. Basic fibroblast growth factor can mediate the early inductive events in renal development. Proc Natl Acad Sci U S A. 1995 May 9;92(10):4696–4700. doi: 10.1073/pnas.92.10.4696. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Peters K., Werner S., Liao X., Wert S., Whitsett J., Williams L. Targeted expression of a dominant negative FGF receptor blocks branching morphogenesis and epithelial differentiation of the mouse lung. EMBO J. 1994 Jul 15;13(14):3296–3301. doi: 10.1002/j.1460-2075.1994.tb06631.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- RAWLES M. E. TISSUE INTERACTIONS IN SCALE AND FEATHER DEVELOPMENT AS STUDIED IN DERMAL-EPIDERMAL RECOMBINATIONS. J Embryol Exp Morphol. 1963 Dec;11:765–789. [PubMed] [Google Scholar]
- Riddle R. D., Johnson R. L., Laufer E., Tabin C. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell. 1993 Dec 31;75(7):1401–1416. doi: 10.1016/0092-8674(93)90626-2. [DOI] [PubMed] [Google Scholar]
- SENGEL P., ABBOTT U. K. IN VITRO STUDIES WITH THE SCALELESS MUTANT. INTERACTIONS DURING FEATHER AND SCALE DIFFERENTIATION. J Hered. 1963 Nov-Dec;54:255–262. doi: 10.1093/oxfordjournals.jhered.a107261. [DOI] [PubMed] [Google Scholar]
- Song H. K., Sawyer R. H. Dorsal dermis of the scaleless (sc/sc) embryo directs normal feather pattern formation until day 8 of development. Dev Dyn. 1996 Jan;205(1):82–91. doi: 10.1002/(SICI)1097-0177(199601)205:1<82::AID-AJA8>3.0.CO;2-1. [DOI] [PubMed] [Google Scholar]
- Stern C. D., Yu R. T., Kakizuka A., Kintner C. R., Mathews L. S., Vale W. W., Evans R. M., Umesono K. Activin and its receptors during gastrulation and the later phases of mesoderm development in the chick embryo. Dev Biol. 1995 Nov;172(1):192–205. doi: 10.1006/dbio.1995.0015. [DOI] [PubMed] [Google Scholar]
- Vaahtokari A., Aberg T., Jernvall J., Keränen S., Thesleff I. The enamel knot as a signaling center in the developing mouse tooth. Mech Dev. 1996 Jan;54(1):39–43. doi: 10.1016/0925-4773(95)00459-9. [DOI] [PubMed] [Google Scholar]
- Vainio S., Karavanova I., Jowett A., Thesleff I. Identification of BMP-4 as a signal mediating secondary induction between epithelial and mesenchymal tissues during early tooth development. Cell. 1993 Oct 8;75(1):45–58. [PubMed] [Google Scholar]
- Zúiga Mejía Borja A., Meijers C., Zeller R. Expression of alternatively spliced bFGF first coding exons and antisense mRNAs during chicken embryogenesis. Dev Biol. 1993 May;157(1):110–118. doi: 10.1006/dbio.1993.1116. [DOI] [PubMed] [Google Scholar]